Atmospheric Change and the Diversity of Aquatic Invertebrates: Are We Missing the Boat?

ATMOSPHERIC CHANGE AND THE DIVERSITY OF AQUATICINVERTEBRATES: ARE WE MISSING THE BOAT?

IAN D. HOGG1;3, JOHN M. EADIE2 and YVES DE LAFONTAINE11 Centre Saint-Laurent, Environment Canada, 105 McGill, Montreal, QC, Canada H2Y 2E7;

2 Dept. of Wildlife, Fish and Conservation Biology, University of California, Davis, CA 95616,U.S.A.;3 Present address: Dept. of Biological Sciences, University of Waikato, Private Bag 3105,

Hamilton, New ZealandE-mail: [email protected].;

(Received in final form 12 September, 1996)

Abstract. The response of natural systems to atmospheric change may depend critically on speciesdiversity and on the genetic diversity (variability) found within their respective populations. Yet, mostsurveys of aquatic invertebrates account for neither. This may be of particular concern for benthicpopulations in running waters because of the considerable variability and the fragmentary natureof these habitats (e.g. isolated watersheds). In such habitats, species with limited genetic variabilityand/or limited dispersal capabilities (genetically differentiated populations) may be unable to trackrapid environmental change, and may be more susceptible to climatic perturbations. We present aconceptual framework to illustrate some of the potential problems of ignoring population geneticswhen considering the impacts of global atmospheric change. We then review a simple method toassess population genetic structure and we evaluate available data on the genetic structure of NorthAmerican stream invertebrates. These data indicate that benthic taxa often consist of genetically differ-entiated local populations, or even previously unknown species. Accordingly, our limited knowledgeof population structure among benthic invertebrates may result in the unwitting loss of genetic and/orspecies diversity. Enhanced taxonomic research incorporating molecular techniques is clearly war-ranted. Conservation strategies based on the preservation and remediation of a diversity of aquatichabitats are likely to be our best means of ensuring species and genetic diversity of invertebrate taxa.

Key words: benthic invertebrates, biodiversity, conservation, genetic differentiation, global change,lotic systems, population genetics

A biologist who assumes that he is studying a single species when in facttwo or more are involved runs the risk of grossly misinterpreting his data,(Richardsonet al., 1986).

1. Introduction

Global atmospheric change may result in one of the most rapid climatic shifts expe-rienced by the earth’s biota in the past 2 million years (Jaeger, 1988). Such changesmay result in considerable short-term disruption for the inhabitants of aquaticecosystems (Regieret al., 1990; Hogg and Williams, 1996). However, the long-term response of natural systems to large spatial and temporal scale atmosphericchanges (e.g. acid deposition, global warming) may depend critically on speciesdiversity and on the genetic diversity (variability) found within their respectivepopulations. A considerable research effort has therefore been undertaken to eval-uate genetic differences among fish taxa, with the view to defining ‘evolutionarysignificant units’ (see Gharrettet al., 1994; Nielson, 1995, and papers contained

Environmental Monitoring and Assessment49: 291–301, 1998.c 1998Kluwer Academic Publishers. Printed in the Netherlands.

292 IAN D. HOGG ET AL.

therein). By comparison, most surveys of aquatic invertebrates account for nei-ther species diversity nor genetic diversity. This may be of particular concern forbenthic populations in lotic (running-water) systems because of the considerablespatial and temporal variability of the physical, chemical and biological featuresthat exist within habitats, as well as the discrete, often fragmentary nature of theirhabitats. Accordingly, populations may become genetically distinct at the race,subspecies or even species level, each adapted to local conditions (Slatkin, 1987).Unfortunately, morphologically based classification schemes (e.g. taxonomy) maynot accurately represent true species (Dillon and Davis, 1980). This may be furthercompounded by a decline in taxonomic research as well as the level of expertiserequired in identifying known taxa to the species level. These issues have seriousconsequences for the maintenance of species diversity within aquatic habitats – ourfailure to account for any unique genetic stock may result in its unintentional loss.

Here we present a conceptual framework to illustrate some of the potential con-sequences of ignoring population genetics in view of impending global atmospher-ic change. We describe one of the methods available to assess genetic diversity innatural populations and we review data on population genetic structure for NorthAmerican stream taxa. Our results suggest that consideration of the genetic diversi-ty of aquatic invertebrates should be an important consideration in the managementand conservation of lotic systems.

2. Population Genetic Structure and Atmospheric Change

A tenet of evolutionary theory is that species with greater levels of genetic variabil-ity may be able to inhabit a wider range of environmental conditions, and hencewould be better able to adapt to environmental change relative to species withlower genetic variability (Figure 1A). Consequently, much concern has focused onthe maintenance of genetic variation (heterozygosity) in natural populations. How-ever, the partitioning of this variation among populations within species (‘geneticdifferentiation’) may also be crucial. For example, although two species may havesimilar levels of overall genetic variability, the variability that exists within anygiven population may be quite low (e.g. species ‘b’, Figure 1B). The extent towhich populations of a species become differentiated will be determined, in part,by the biological characteristics of the species (e.g. dispersal abilities/gene flow,geographic distribution), as well as by any selective pressures/events that have beenimposed on the local populations (Hedrick, 1986). For running water ecosystemswhich often consist of discrete, naturally fragmented habitats (e.g. separate water-sheds) with highly variable physical, chemical and biological characteristics, bothfactors are likely to play significant roles.

To illustrate the potential ramifications of different population genetic structuresrelative to atmospheric change, consider four hypothetical species (‘a, b, c, d’)differing in levels of genetic variability within their local populations (‘x, y, z’)

ATMOSPHERIC CHANGE AND THE DIVERSITY OF AQUATIC INVERTEBRATES 293

Figure 1. Graphical representation of possible scenarios for genetic variability (within species)and genetic differentiation occurring among populations. A) Distribution of 2 hypothetical speciesalong an environmental continuum. Species ‘a’ has high levels of genetic variability and occupies awider range of environmental conditions versus species ‘b’. B) Distribution of 2 hypothetical speciesoccupying a similar range of environmental conditions, but differing in the differentiation of threepopulations (x, y, z) along the continuum.

as well as in their dispersal abilities (gene flow) among populations (Figure 2).We will assume that species ‘a’ and ‘b’ have greater levels of overall geneticvariability than species ‘c’ and ‘d’, and that species ‘b’ and ‘d’ have greaterlevels of differentiation among their respective populations resulting from lowerlevels of gene flow. Following an atmospheric change that eliminates part of theenvironmental continuum inhabited by the four species (shaded area), only species‘a’ maintains the genetic diversity found within its local populations. Species ‘c’and ‘d’ are eliminated entirely, while species ‘b’ incurs the extirpation of localpopulations (i.e. population ‘x’) and hence the loss of genetic diversity. Althoughspecies ‘b’ persists following the atmospheric change, its ability to respond tofuture, or concomitant, perturbations may be reduced. Accordingly, for specieswith limited genotypic variation (e.g. species ‘c, d’) or strong differentiation (e.g.,


Figure 2. Graphical representation of the genetic structure for four hypothetical species (a–d),differing in levels of genetic variability and differentiation among three populations (x, y, z) alongan environmental continuum. An atmospheric change which eliminates part of the environmentalcontinuum occupied by the species is indicated by the shaded area.

species ‘b’), the ability to track rapid environmental change may be much morerestricted relative to species with higher genetic variation and greater gene flowamong sites (e.g. species ‘a’). Any attempt to assess the ecological consequences ofdirectional shifts in climatic conditions clearly requires that both genetic diversityand differentiation be considered.

3. Assessing the Genetic Structure of Stream Invertebrates

Several methods have been used to evaluate the genetic structure and speciesboundaries for natural populations, including laboratory experiments (e.g. Strong,1972) and morphological analysis (e.g. Wellborn, 1994). Recent developments inmolecular genetics have provided a new and powerful toolkit for field biologistsand information on the genetic structure of populations is now being generatedat a level of resolution previously unavailable (Avise, 1994). However, many ofthese methods are expensive, are technologically demanding, and require accessto a fully-equipped molecular laboratory. Fortunately, some techniques, such asallozyme electrophoresis, are relatively inexpensive, and require only minimal lab


facilities and procedures for rapid and efficient screening of populations. Allozymeanalysis allows identification of the alleles coding for target enzymes within anindividual organism through the separation of the components responsible for theparticular enzyme according to molecular charge. Several media have been usedto facilitate this separation including starch, acrylamide, and cellulose acetate-based gels. Techniques employing cellulose acetate-based gels may be particularlyappealing for studies of aquatic invertebrates because of the limited amount ofmaterial required to assess several enzyme systems simultaneously and becauseof the ease and speed with which samples can be processed (Hebert and Beaton,1993). Further details on electrophoresis techniques are provided in Harris andHopkinson (1976), Richardsonet al. (1986), and Hebert and Beaton (1993).

To enable comparisons among locations, individual animals from each locationare screened for alleles that code for common enzyme systems. By summing theresults for all individuals at each location, allele frequencies can then be deter-mined. The relative frequencies of alleles among locations then enable an estimateof the relative genetic similarities of the respective populations. Four measuresare frequently used to compare allele frequencies among populations: Nei’s (1972)genetic identity, Rogers’ (1972) genetic distance, Nei’s (1978) unbiased genetic dis-tance, and Wright’s (1978) FST . With the exception of Nei’s (1972) genetic identity,all measures increase in value with greater genetic differences among populations,with values of zero indicating no genetic difference. For example, Wright’s (1978)FST values of 0–0.05, 0.05–0.15, 0.15–0.25, and>0.25 are considered to representlow, moderate, great and very great levels of genetic differentiation among pop-ulations, respectively. For Nei’s (1972) identity, values of 1 indicate populationswith identical frequencies of alleles and 0 indicates populations with no commonalleles. Populations with ‘fixed’ differences in their allele frequencies (i.e. havingalleles that are not shared with other populations) are usually considered as separatespecies, particularly if occupying the same geographic distribution (Jackson andResh, 1992).

4. A Review of Available Data

A survey of the literature was undertaken to identify studies evaluating the popula-tion genetic structure of North American stream invertebrates. We were particularlyinterested in those studies evaluating the levels of genetic differentiation amongpopulations. For each paper, we noted the geographic scale involved, the relativeisolation of the habitats, and the extent of differentiation among habitats.

We found 20 published papers and 2 unpublished studies representing 5 insectorders, 2 non-insect orders, and covering roughly 35 currently recognised ‘species’.A majority (59%) of the studies focused on only two taxonomic groups (Amphipo-da: Crustacea, and Ephemeroptera: Insecta). A summary of all studies together with


information on the levels of genetic differentiation among populations is providedin Table I.

The spatial scale of the studies varied considerably with some studies examiningdiscrete habitats within a local area (e.g. 5 km; Gooch and Hetrick, 1979), andothers looking at relatively continuous habitats over much larger scales (e.g. theSt. Lawrence River, Hogget al., unpubl. data). For 23 of the 35 taxa (66%),moderate to great levels of differentiation among populations were reported. Thiswas particularly evident for species occupying discrete habitats and for species withlimited dispersal capabilities (e.g. Ephemeroptera, Gastropoda, and Amphipoda).High levels of differentiation were found in some populations that were separatedby less than 5 km (e.g. Kaneet al., 1992). Three of the studies reported a total of 12previously unidentified ‘cryptic’ species. Clearly, benthic invertebrate populationstend to be highly structured genetically.

5. Discussion and Conclusions

The rapid climatic shifts anticipated as a result of global atmospheric change (e.g.Jaeger, 1988), will be in addition to a considerable range of concomitant pressuresincluding acid deposition, habitat destruction and fragmentation. Accordingly, thechallenges to natural systems are considerable. Based on our review of a limitednumber of North American stream invertebrates, we suggest that variability withinmany populations of stream invertebrates, and hence their ability to respond maybe limited. A majority of the studies we surveyed found evidence for moderate tovery-great levels of genetic differentiation (sensuWright, 1978) among populationsof stream invertebrates. Indeed, in three of the studies (Funket al., 1988; Sweeneyand Funk, 1991; Jackson and Resh, 1992), 12 previously unknown species werefound – a value equivalent to almost one third (31%) of the previously recognisedspecies that were initially studied. It is highly probable that many unstudied taxa(particularly widespread species) will consist of one or more sympatric or allopatricspecies.

The implications for those concerned with conservation of natural speciesassemblages are twofold. First, our current strategy of identifying species on thebasis of gross morphological characteristics (taxonomy) may be misleading. Thefact that so many ‘cryptic’ species were identified using allozyme analyses sug-gests that our current inventory of aquatic invertebrates is not only incomplete,but perhaps grossly underestimated. Without better methods to account for speciesdiversity in the true sense (i.e. reproductively isolated units), our hopes of monitor-ing changes in biodiversity in response to climate change may be futile. Second,our survey suggests that simply documenting the existence of species within agiven geographic region will provide little information on the ability of that speciesto persist following an atmospheric change. Predicting the long-term viability of aspecies will require knowing not only its current distribution, but also the patterns


Tabl

eI

Nor

thA

mer

ican

stre

amta

xafo

rw

hich

data

onpo

pula

tion

gene

ticst

ruct

ure

are

avai

labl

e

Taxo

nA

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r(s)

Diff

eren

tiatio

nam

ong

popu

latio

nsa

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cta

Eph

emer

opte

raD

ola

nia

am

erica

na

Sw

eene

yan

dF

unk,

1991

mod

erat

e-gr

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sout

hea

ster

nN

A,F

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=0.

059–

0.36

4,cr

yptic

sp.

Ephem

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llaaurivi

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Sw

eene

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l.,19

87m

oder

ate

with

inno

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east

ern

NA

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nF

ST

=0.

153

E.s

epte

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ionalis

Sw

eene

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l.,19

87lo

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ithin

east

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NA

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=0.

036

E.s

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eene

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l.,19

86lo

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ithin

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aina

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sin,

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028

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068

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1987

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Tabl

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ong

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tera

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sim

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n,19

84m

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gan,

mea

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096

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der

and

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1984

low

with

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003

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l.,19

89m

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gla

ban

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tions

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295

Tric

hopt

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osp

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son

and

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h,19

92gr

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N=

0.39

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yptic

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d

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of genetic diversity and differentiation found among populations of that species(e.g. Figure 2). Species with limited genetic variability and/or limited dispersalcapabilities (genetically differentiated populations) may be unable to track rapidenvironmental change, and may be highly susceptible to climatic perturbations.

Why might the genetic variability of aquatic invertebrates be limited? Possibly,strong selection forces operate in running-water habitats, resulting in a loss of‘unfit’ genotypes. Variation in the intensity or the direction of selection amonghabitats could promote local adaptation and reduced genetic variability withinpopulations, but could lead to increased differentiation among populations. Kaneet al. (1992) suggested that such a scenario may account for the high degree ofdifferentiation observed inGammarus minus(Amphipoda) collected from highlydivergent cave and surface streams (see also Sarbu and Kane, 1993). However,an alternative explanation is possible (Kaneet al., 1992) – gene flow amongpopulations in isolated lotic habitats may be severely restricted, resulting in the lossof genetic variants within habitats, and increased differentiation among habitats,due to random genetic drift. Consistent with this hypothesis, our survey indicatedthat levels of genetic differentiation were greatest among species with limiteddispersal capabilities (e.g. Dillon and Davis, 1980) and those occupying spatiallyisolated streams of increasing separation (e.g. Sweeneyet al., 1992; Table I).

In summary, we emphasise that our current methods of assessing diversityamong stream invertebrates may be limited, and perhaps misleading. Although wedo not yet fully understand the evolutionary mechanisms generating the observedpatterns of population genetic structure, our review of the published literatureindicates that many currently recognised stream invertebrate taxa are geneticallydistinct at the race, subspecies and species levels. Accordingly, to maximise ourprospects of sustaining aquatic biodiversity in the face of climatic change, wesuggest three areas for future attention: 1) additional research on the taxonomyof aquatic invertebrates, particularly employing molecular techniques, in orderto better inventory existing patterns of biodiversity; 2) analyses of populationgenetic structure for a wider range of stream invertebrates to assess levels ofgenetic variability and differentiation within species; and 3) examination of theinter-habitat dispersal abilities for a range of aquatic invertebrates. Until suchinformation becomes available, conservation strategies based on the preservation,and remediation, of a diversity of aquatic habitats will likely be our most effectivemeans of ensuring both species diversity and genetic diversity of stream invertebratetaxa. If we fail to consider such factors, we may not only be missing the boat, butpossibly the Ark as well.

Acknowledgements

We thank F. Boudreault for assistance drafting Figures 1 and 2. Logistic supportfor unpublished data contained in Table I was provided through NSERC operating


grants to J. M. Eadie and D. D. Williams, and the St. Lawrence Vision 2000 Plan(Environment Canada). I. Hogg was supported through a Visiting Fellowship in aCanadian Government Laboratory.

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